I dedicate this work to my grandparents: Adriana Gertrude (Jane) Tims Paulson Willard (Bill) Paulson Merwin Oyen Karen (Kay) Kleven Oyen
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1 Acknowledgments First and foremost, I'd like to thank my advisors, Ching-Chang Ko and E. Russell Ritenour, for support and encouragement to complete this degree. I owe a great debt of gratitude to the Queen Mary, University of London group, headed by Andy Bushby, and including the great Alan Boyde, Aman Bembey, and Ginger Ferguson. Their data, generously provided, made a significant difference in this work; I am also indebted to them for many long discussions of mineralized tissues. Special thanks to Andy Liu, for performing the original bone indentation tests associated with this project. Thanks also to Warren Oliver, Jenny Hay, and Erik Herbert at MTS Nano, and Oden Warren at Hysitron. Finally, other colleagues, here and elsewhere, with whom I have had invigorating technical discussions on topics more-or-less related to this work include Y.T Cheng, Robert Cook, Eve Donnelly, Ravi Nalla, Wook-Jin Seong, and Mike Swain. i
2 I dedicate this work to my grandparents: Adriana Gertrude (Jane) Tims Paulson Willard (Bill) Paulson Merwin Oyen Karen (Kay) Kleven Oyen ii
3 Abstract Recent developments in instrumentation have increased the use of contact mechanical testing techniques ( nanoindentation ) for the examination of local mechanical responses. These techniques are ideal for testing tissue biomechanical responses on the scale of the tissue ultrastructure. However, features of the mechanical response of tissues, such as time-dependence and inhomogeneity, add complexity to the analysis of indentation testing. The current work is aimed at promoting understanding of mechanics of biological tissues at the level of the ultrastructure. Engineering materials with known composition and properties are used as model materials for exploring the indentation mechanical behavior of time-dependent and inhomogeneous systems. Modeling techniques, both analytical and computational, are used to understand the fundamental mechanical behavior of biological composite material systems at ultrastructural lengthscales. Models of mineralized tissue behavior at small scales are developed for both homogeneous and indentation loading. After establishing the mechanics framework for investigating these material types, indentation experiments are performed on biological materials and mechanical properties are extracted using the models that have been developed. Techniques developed in the current work are used to examine variations in mechanical response of healing bone as a function of distance from the dental implant interface and as a function of healing time since implantation. Relative contributions of mineral content and local mineral network structure on variations in elastic modulus were examined. iii
4 Table of Contents Chapter 1: Introduction Statement of Problem Materials Background Engineering Materials and Mechanical Behavior Bone Bone Composition Bone Hierarchy and Microstructure Bone Phase Continuity Bone Healing and Remodeling Mechanical Behavior of Bone Mineralized Tooth Tissues Enamel Dentin Tooth Replacement via Dental Implants Road Map of this Work Chapter 2: Mechanics Background Contact Mechanics and Indentation Testing Indentation Testing Advantages Spherical Indenter (Hertzian) Solutions Conical Indenter Solutions Oliver-Pharr Analysis Experiment Types for Indentation Testing Indentation Testing Instruments MTS Nanoindenter XP Hysitron Triboscope/Triboindenter Time-Dependent Mechanical Behavior Model-Independent Measures of Time-Dependence Viscoelastic Spring-Dashpot Models Linearly Viscoelastic Behavior Mechanical Properties of Composite Materials Physical Properties of Composite Materials Elastic Modulus of Composite Materials Finite Element Analysis Introduction and Discretization Fully 3D Problems Plane Strain Problems Mechanical Directions for this Work iv
5 Chapter 3: Elastic-Plastic Indentation Experiments Elastic-Plastic Indentation Analysis Calibration Typical Area Function Calibration Frame Compliance Effects in Calibration Compliant Material Calibration Issues Calibration Standards for Compliant Materials Oliver-Pharr Analysis and the Contact Displacement Elastic-Plastic Bone Indentation Bone-Dental Implant Study Methods Effect of Instrument and Calibration Effect of Bone Healing Time Nanoindentation Variability Experiments Homogeneous Controls Biological Composites Summary of Indentation Variability Property Mapping Mapping the Dentin-Enamel Junction Bone Modulus Mapping Discussion Chapter 4: Time-Dependent Indentation Time-Dependent Effects in Indentation Testing Hallmarks of Indentation Creep Indentation Creep in Mineralized Tissues Viscoelastic Indentation by Radok Correspondence Nonlinearly Viscoelastic Indentation Mechanics Creep Following Ramp Loading The VEP model Model Adaptation of the VEP Model to Routine Testing Time-Dependent Indentation Experiments on Mineralized Tissues VEP Analysis of Dentin Hydration VEP Analysis of Healing Bone Implications of Viscosity-Modulus Correlations VEP Comparison of Bone and Dentin Discussion v
6 Chapter 5: Modeling Bone as a Two-Phase Composite Mineralized Tissues as Composite Materials Mineral Volume Fractions Mineral Phase Elastic Properties Organic Phase Elastic Properties FEA Model for Homogeneous Loading Anisotropy: Particle Shape and Distribution Variations Anisotropy Model FEA Comparison with Halpin-Tsai Examination of the Stiffening Mechanism in High-AR Composites Modeling of Interpenetrating Phase Composites Porosity and Collagen Modulus Effects Intermediate connectivity Intermediate Connectivity in 1D Intermediate Connectivity in 2D Discussion Chapter 6: Modeling and Bone Indentation Scaling Laws for Indentation of Particulate Composites FEA Model for Inhomogeneous Indentation Model Validation for Indentation Loading Model for Indentation Loading of a Composite Indentation Model Applied to Bone and Dentin Examination of Bone Indentation Variability Background Conversion to Composite Materials Framework Estimates of Bone Structure from Modulus Embedded bone Background Analysis Discussion Chapter 7: Discussion and future work Discussion Indentation Testing Mineralized Tissues as Composite Materials Implications of Bone Variability Conclusions vi
7 Appendix A: Gelatin-Apatite Composites A.1 Biomimetic Composites for Modeling Bone A.1.1 Bone Tissue Engineering A.1.2 Biomimetic Composite Fabrication A.2 Variability in Gelatin-Apatite Composites and Components A.2.1 Components A.2.2 Composites A.2.3 Materials Variability and Modulus Comparison A.3 Composite Bounds and the Modulus of Gelatin-Apatite Composites Appendix B: Indentation Contact Hardness B.1 Contact Hardness background B.1.1 Vickers Indentation B.1.2 Contact Hardness in Nanoindentation B.2 Elastic-Plastic Contact Hardness B.2.1 Series Model B.2.2 Elastic-Plastic Materials Analysis B Engineering Materials B Dentin B Implications for Bone B.3 Viscous-Elastic-Plastic Contact Hardness B.3.1 Series Model B.3.2 Estimation of Material Time-Constant from Contact Hardness... 2 B.3.3 Contact Hardness Calculations for Time-Dependent Materials B PL-1 Polymer B Bone vii
8 List of Tables Table 1-1: Isotropic elastic properties for common engineering materials... 9 Table 3-1: Means and standard deviations for modulus and hardness of bone Table 3-2: Small-depth indentation modulus variability Table 3-3: Large-depth indentation modulus for variability studies Table 4-1: PL-1 properties from VEP fits Table 4-2: Mechanical properties from dentin indentation Table 4-3: Averages of parameters for the VEP fits of data shown in Fig Table 4-4: Average deformation components for the data in Tables 4-1 and Table 5-1: Mineralized tissue mean composition by weight or by mass density Table 5-2: Mineralized tissue volume fraction based on data in Table Table 5-3: Phase fraction calculated for FEA meshes with different particle spacing Table 5-4: Summary of finite element simulations run in the current study Table 5-5: Isotropy or anisotropy in different FEA meshes Table 5-6: 3D Unit cell FEA results for the structures of Figure Table 5-7: Comparison of models for compliant collagen or a void phase Table 5-8: Volume fractions of mineral for different interparticle spacing Table 5-9: Effective modulus results for partially-connected structures Table 6-1: Mean and ranges of mineral fraction and elastic modulus in bone Table 6-2: Indentation moduli and anisotropy ratio for bone Table 7-1: Coefficient of variation for modulus from different analyses... 2 Table A-1: Small-depth variability for component and composite materials... 2 Table A-2: Large-depth convergence for component and composite materials... 2 Table A-3: Gelatin-apatite component and composite moduli... 2 Table B-1: Plastic deformation resistance for engineering materials... 2 Table B-2: Relative proportions of elastic and plastic deformation... 2 Table B-3: Property averages for indentation tests near to and far from the DEJ... 2 Table B-4: Plastic deformation resistance calculated for data in Table B Table B-5: Time constants and exponential decay constant fits... 2 Table B-6: Contact hardness calculated for PL-1 using data in Table viii
9 List of Figures 1-1: Uniaxial tension testing geometry : Uniaxial stress-strain curves for three material types : Mechanical response of aluminum under tensile loading : Time-dependent creep and relaxation responses under fixed loading : Viscoelastic stress-strain response sfor constant rate loading at two rates : Collagen periodic banding : Collagen cross-linking : Apatite crystal structure : Bone mineralzation by apatite crystal nucleation and growth : Quantification of the scales of bone hierarchy, after Weiner and Wagner : Ultrastructural lengthscales of bone (from nm to mm) : Stress-strain responses for cortical and trabecular bone : Strain-rate effects on bone mechanical stress-strain responses : Stress-strain responses of demineralized bone : Tooth and Jawbone anatomy and relationships : The dentin-enamel junction (DEJ) : Collagen network around the dentinal tubules : Dental implant anchored into bone : Osseointegration in dental implants and the bone-implant interface : Mechanically tested volume of material for tensile and contact testing : Profile (transverse section) of conical/pyramidal and spherical indenter tips : Contact projected area as a function of tip displacement for indenter tips : Indentation tests performed on three classes of materials two indentation tips : Perfectly elastic spherical indentation data for glass : Spherical indentation data for purely elastic contact : Spherical indentation data for elastic-plastic contact : Berkovich pyramid indenting a deforming surface, contact depth : Berkovich indentation data for quadratic load-displacement behavior : parameters obtained directly from the raw load-displacement data : Reduced modulus as a function of sample plane-strain modulus : Common load-time testing inputs for nanoindentation contact mechanical tests : Schematic diagram of the MTS Nanoindenter XP : Schematic diagram of the Hysitron indentation system : Schematic diagram of Relaxation elastic fraction or total creep displacement : Schematic diagram of Hysteresis energy : Linear Hookean spring and Newtonian Dashpot mechanical elements : Simple combinations of spring and dashpot elements give viscoelastic models : Elastic Modulus bounds for modulus mismatch factors of 10, 100, or : Domain discretization in one dimension (left) and two dimensions (right) : Elastic modulus versus depth for fused silica using continuous stiffness : Plane strain modulus vs depth for polyurethane using continuous stiffness : Peak displacement, stiffness and contact displacement for fused silica : Contact area for fused silica for different values of the frame compliance ix
10 3-5: Area function fitting for different assumed values of frame compliance : First and second terms of the area function as a function of frame compliance : Modulus and hardness for fused silica with different frame compliance : Plot of the complete area function and the individual component terms : Nanoindentation depth-dependence of the elastic modulus of a polymer : Three bone samples harvested from bone along the dental implant interface : Modulus vs distance from the bone-implant interface [Chang et al, 2003b] : Plane strain modulus from the original study and after re-calibration : Modulus for the same samples tested with two indentation instruments : Modulus versus distance from interface for indentation tests at 1, 2, 4 months : Frequency histograms for modulus values at different time points healing : Raw indentation responses for fused silica at three peak load levels : Elastic modulus for the fused silica indentation tests shown in Figure : Elastic modulus data for single crystal mineral apatite : Variability in bone indentation modulus at different peak load levels : Variability in indentation modulus of mineralized tooth tissues : Cross section of a tooth (3rd molar) illustrating the indented region : Composite image of the indented area in a tooth : Raw indentation traces for tests across the dentin-enamel junction : Plane strain elastic modulus map of the dentin-enamel junction : Plane strain elastic modulus overlay map of the dentin-enamel junction : Raw indentation load-displacement traces for indentation tests on healing bone (a): Composite optical image for bone specimen following one month healing (b): Plane strain elastic modulus map for 1-month sample in 3-27(a) (c): Overlay image of the combined optical and mechanical information (a): Composite optical image for bone specimen following two months healing (b): Plane strain elastic modulus map for 2-month sample in 3-28(a) (c): Overlay image of the combined optical and mechanical information (a): Composite optical image for bone specimen following four months healing (b): Plane strain elastic modulus map for 4-month sample in 3-29(a) (c): Overlay image of the combined optical and mechanical information : Frequency histograms for modulus values after bone healing 1, 2, 4 months : DEJ modulus map (Figure 3-25) with the scale set to that used for bone maps : Indentation load-displacement and creep displacement-time responses : Indentation response at slow rate to illustrate apparently negative stiffness : Indentation load-displacement responses for PMMA at three rise times : Contact hardness deconvoluted from PMMA indentation at three rise times : Residual impressions for PMMA, tested at rise times of 5 s, 50 s, and 500 s : Bone creep load-displacement and creep displacement-creep time responses : Dry dentin indentation load-displacement responses for tests at three rates : PL-1 polymer indentation ramp-hold creep displacement-time data for four rates : Data from the load-hold portion of the PL-1 polymer data shown in Fig : Unloading displacement-time and load-displacement data for PL-1 indentation : Indentation load-displacement responses for dry and wet dentin : Normalized indentation responses for dry and wet dentin : Displacement-time and load-displacement traces for indentation on bone x
11 4-14: VEP parameters as a function of distance from the bone-implant interface : The range of bone indentation responses obtained in the current study : Direct dependence of VEP viscosity on modulus : Two indentation load-displacement traces generated from the VEP model : Load-displacement traces for dry bone and dentin, tested in the same conditions : Elastic modulus bounds and mineralized tissue composite behavior : Stress-strain plot for four levels of collagen organization [An et al, 2004] : Finite element model of two-phase composite, loaded homogeneously : Effective elastic modulus computed for FE tensile loading of composites : Geometric identifiers for finite element models : Effectve modulus as a function of mineral volume fraction for square particles : Composite elastic modulus in anisotropic particle composites : Anisotropy ratio as a function of particle aspect ratio : Results from FEA and Halpin-Tsai empirical expressions for whiskers : Calculated effective modulus for a random orientation composite : Effective elastic modulus as a function of particle length fraction : Staggered particle model of Jager and Fratzl [2000] and Gao et al [2003] : Comparison of composite bounds and anisotropic finite element results : 3D finite element model geometries for varied phase continuity : 3D rendering of 2-phase IPC FE model with one phase void : Effect of compliant phase modulus on Hashin-Shtrikman bounds : Schematic illustration of bounds and corresponding structures : Interrupted fiber model for examining partially connected composite materials : Modulus values for interrupted fiber model and the Voigt-Reuss bounds : Illustration of the parameters used to estimate connectivity from modulus : Connectivity fraction calculated from geometry and estimated from modulus : Three-component model with matrix, particles, and inter-particle connectors : Schematic illustration of connectivity indices Ci : Composite modulus results for four configurations shown above in Fig : Schematic illustration of intermediate values of the connectivity indices Cx : Intermediate connectivity for the removal of single linkages or whole rows Variation in the modulus with mineral fraction for different connectivity : Calculated connectivity fraction for the data shown in Figure : Variation in the composite modulus with mineral phase connectivity : Partially-connected composites arranged in all possible configurations : Proposed structural model of bone based on the observed mineral geometry : 2D and 3D unit cells for a single circular or spherical particle : Particles displaced by a Berkovich indenter as a function of displacement : The contact width equivalence for Berkovich and flat punch indentation : Schematic illustration of indentation model boundary conditions : Pressure profile from flat punch indentation FE model of a homogeneous solid : Comparison of tensile and indentation finite element results : Centering of flat punch indent over particle or matrix : Line load-displacement responses from FEA flat punch indentation : Effective elastic modulus from indentation FEA models for composite materials xi
12 6-10: Effective modulus for different indent locations at increasing indent depth : Comparison of bone indentation data with indentation finite element model : Comparison of dentin indentation data with indentation finite element model : Indentation modulus versus qbse mineralization [Ferguson et al, 2003] : Indentation elastic modulus versus mineral fraction for subchondral bone : Modulus data averaged for volume fraction in increments of 0.01 and line fit : Average bone modulus data with the Hashin-Shtrikman bounds : Histograms of observed modulus values for mineral fractions of 0.43 to : Mean and range of calculated connectivity fraction for subchondral bone : Data from Figure 5-8 compared with the measured anisotropy ratio for bone : Structures representing a composite with connected or disconnected mineral : Hashin-Shtrikman modulus bounds for a composite of PMMA and apatite : Illustration of structures with different mineral phase connectivity : Elastic modulus map of a portion of bone-implant interface : Schematic diagram of an axisymmetric bone-implant finite element model : Assignment of modulus values in heterogeneous FEA model of bone : Shear strain map for FEA model of bone assuming bone homogeneity : Shear strain map for FEA model of bone assuming bone heterogeneity : Shear strain map for FEA model of bone assuming bone heterogeneity... 2 A-1: Variability in elastic modulus values for gelatin and polycrystalline apatite... 2 A-2: Indentation responses for small load levels on a gelatin-apatite composite... 2 A-3: Variability in modulus values with peak load for gelatin-apatite composites... 2 A-4: Variability in modulus values for a gelatin-apatite composite... 2 A-5: Gelatin-apatite composites have modulus values closest to the lower bounds... 2 B-1: Vickers Indentation schematic illustration... 2 B-2: Illustration of elastic recovery in a transverse section of indentation impression... 2 B-3: Vickers indentation residual impression in hydroxyapatite and composite C... 2 B-4: Contact hardness for hydroxyapatite and gelatin-apatite composite C... 2 B-5: Property gradients with distance from the dentin enamel junction... 2 B-6: Calculated contact hardness versus plane strain modulus... 2 B-7: Calculated contact hardness versus rise time for four values of viscosity... 2 B-8: Oliver-Pharr contact hardness as a function of rise time for polymers... 2 B-9: Modulus, plastic deformation resistance and contact hardness relationships... 2 xii
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